A study of the cortical processing of ano-rectal sensation using functional MRI

Abstract

Investigation of human ano-rectal physiology has concentrated largely on understanding the motor control of defecation and continence mechanisms. However, little is known of the physiology of ano-rectal sensation. There are important differences in the afferent innervation and sensory perception between the rectum and anal canal. This suggests that there could also be differences in the brain's processing of sensation from these two areas; however, this possibility remains unexplored. The aim of our study was to identify the cerebral areas processing anal (somatic) and rectal (visceral) sensation in healthy adults, using functional MRI. Eight male subjects with an age range of 21-39 years were studied on two separate occasions, one for rectal and the other for anal stimulation studies. Single shot gradient echo planar imaging was performed using a 1.5 tesla Phillips MRI scanner. For each subject, a series of 40 image sets containing 24 slices of the brain was obtained during periods of rapid phasic non-painful distension of the rectum or anal canal, alternating with rest periods, without stimulation. After motion correction, the images were analysed using cross correlation to identify the cerebral areas activated by the stimulus. Rectal stimulation resulted in bilateral activation of the inferior primary somatosensory, secondary somatosensory, sensory association, insular, peri-orbital, anterior cingulate and prefrontal cortices. Anal canal stimulation resulted in activation of areas similar to rectal stimulation, but the primary somatosensory cortex was activated at a more superior level, and there was no anterior cingulate activation. In conclusion, anal and rectal sensation resulted in a similar pattern of cortical activation, including areas involved with spatial discrimination, attention and affect. The differences in sensory perception from these two regions can be explained by their different representation in the primary somatosensory cortex. The anterior cingulate cortex was only activated by rectal stimulation, suggesting that the viscera have a greater representation on the limbic cortex than somatic structures, and this explains the greater autonomic responses evoked by visceral sensation in comparison with somatic sensation.

Mapping of Brain Activations to Rectal Balloon Distension Stimuli in Male Patients with Irritable Bowel Syndrome Using Functional Magnetic Resonance Imaging

“…[61][62][63][64] Furthermore, some studies reported activations in ACC during non-painful visceral distension implicating the role of this region in the control of autonomic visceral responses rather than to pain perception. 18,27,65,66 However, we observed the activations only during painful visceral distension, which might be another reason for the absence of activations in ACC. Activations in the amygdala and hippocampus in female IBS patients during rectal distension suggests an exaggerated emotional arousal network.…”

New technologies to investigate the brain-gut axis

“…Imaging studies have been performed to explore normal brain processes involved in visceral perception, whether liminal or subliminal and its modulation by attention, conditioning and emotion [22,[28][29][30][31] . Several studies have also looked at the role of visceral perception in emotions and cognitive processes such as learning [32,33] .…”

Neuropathophysiology of functional gastrointestinal disorders

“…Methods of brain imaging offer another investigative modality for addressing questions related to abnormal processing of sensory information in the cerebral cortex of IBS patients [84,[94][95][96] . Functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) are now commonly used to study information processing in the higher brain centers that underlie an individual's experience of conscious sensations.…”

“…Beyond the sensory cortices, fMRI and PET images show representation of both somatic and visceral sensation to be similar in the limbic and paralimbic regions of the cortex (e.g. anterior insular, anterior and posterior cingulate, prefrontal and orbitofrontal cortices [94,95] . These areas are known to be involved in the individual's motivational and emotional mood states and in the cognitive components of visceral sensations.…”